For more than half a century, US troops have stood shoulder to shoulder with South Korean forces to deter an attack from the Communist North.
The presence of American infantry just behind the front line was described as a "trip-wire" to guarantee US involvement from day one of any conflict.
But Washington now says that concept no longer makes sense.
The first signs of a change in policy came last year, when the US announced plans to redeploy its forces in safer positions further south.
The troops are due to leave by 2006
Now these plans have been overtaken by proposals for the largest withdrawal of US forces from the peninsula since the 1970s.
The US wants to remove a third of its 37,000 troops by the end of next year.
One of its two infantry brigades is already packing its bags for Iraq - marking a significant reduction in American front-line strength.
It is unclear whether the other brigade will be moved south of the Han river - away from the front-line, as planned - or whether it will also leave the country.
The speed of the proposed withdrawal has taken South Koreans by surprise.
"The timing is very inappropriate," said Park Jin of the conservative Grand National Party.
"We're concerned about a security vacuum at a time when North Korea is pushing ahead with its development of nuclear weapons."
South Korea's government wants any changes to be phased in over several years, to give it time to upgrade its own forces.
South Korea has an army of some 690,000 troops, which dwarfs the number of American ground troops.
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But the US second infantry division will still be missed. It is a formidable modern fighting force - long charged with defending the traditional invasion corridors into the capital, Seoul.
Military analyst Bruce Bennett, of the Rand Corporation in California, said there were doubts in the short term about South Korea's ability to counter the massive artillery threat from its northern neighbour.
"The South Koreans still have equipment that's decades old - there's an anomaly between the society, which is modern and wealthy, and its armed forces," he said.
But US officials insist that improvements in military technology will more than compensate for fewer troops on the ground.
The Pentagon is planning to spend $11bn to modernise its capabilities in South Korea in the coming years.
It insists that reinforcements can be deployed much more quickly now than in the past.
But officials also say it is time for South Korea to take more responsibility for its own defence.
"The United States spends as much $10bn a year on its forces in Korea, but the Korean Government spends only $15bn on its entire defence budget," said analyst Bruce Bennett.
That may have been acceptable when South Korea was a poor country, he said, but now it is the world's 13th largest economy and should do more.
Some analysts argue that the military balance will not be much affected by the American withdrawal.
Not everyone in South Korea will be sorry to see the US troops go
They say the prospect of massive reinforcements from US bases in Japan and America has always been the main deterrent to North Korea - rather than troops on the ground.
Of more concern, they say, is the state of the alliance between Seoul and Washington.
"Anti-American sentiment has given the impression that US troops are not welcome in South Korea - it has contributed to uncomfortable relations between the two countries," said Park Jin.
There is an underlying fear in South Korea that the country is being punished for massive anti-American demonstrations two years ago, after two South Korean school-girls were crushed to death by a US armoured vehicle.
It is clear that the redeployment of forces in Korea is part of a global move by the US to make its forces more flexible.
South Korea would like to be an exception, because of the continued threat from North Korea's million-strong army.
But, stretched thin by the occupation of Iraq, the US army can no longer afford to have one of its divisions tied up permanently on the Korean peninsula.
The US wants its forces in Korea to be available for duties elsewhere in the world.
The changing realities have come as a shock to South Korea, which had come to rely on a seemingly open-ended commitment for American troops to be deliberately placed within range of North Korean guns.